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Allergic Reactions to Anisakis Found in Fish

  • Natalie E. Nieuwenhuizen
  • Andreas L. LopataEmail author
FOOD ALLERGY (D ATKINS, SECTION EDITOR)
Part of the following topical collections:
  1. Topical Collection on Food Allergy

Abstract

The food-borne parasite Anisakis is an important hidden food allergen. Anisakis is a parasitic nematode which has a third-stage larval form that infects mainly fish, and ingestion of contaminated seafood can result in severe allergic reactions. Symptoms experienced due to exposure to this parasite include gastrointestinal disorders, urticaria, dermatitis, asthma and even anaphylaxis. Accurate prevalence data of allergic sensitisation to Anisakis are difficult to estimate due to the lack of well-designed population-based studies. Current diagnostic approaches rely on the detection of serum IgE antibodies to allergenic proteins, which however demonstrate considerable immunological cross-reactivity to other invertebrate allergens. While exposure to this parasite seems to increase due to the increasing consumption of seafood worldwide, the immunology of infection and allergic sensitization is not fully understood.

Keywords

Anisakis Parasite Food allergy IgE antibody Allergen Food-borne 

Notes

Acknowledgments

The authors thank the NRF, South Africa, for financial support and the Australian Biological Resource Study (ABRS) to AL. AL is supported by an ARC Future Fellowship.

Compliance with Ethics Guidelines

Conflict of Interest

Dr. Lopata and Dr. Nieuwenhuizen declare that they have nothing to disclose.

Human and Animal Rights and Informed Consent

This article does not contain any studies

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Smith JW, Wootten R. Anisakis and anisakiasis. Adv Parasitol. 1978;16:93–163.PubMedCrossRefGoogle Scholar
  2. 2.
    Blaxter ML et al. A molecular evolutionary framework for the phylum Nematoda. Nature. 1998;392:71–5.PubMedCrossRefGoogle Scholar
  3. 3.
    Nielsen C. Sequences lead to tree of worms. Nature. 1998;392:25–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Mattiucci S, Nascetti G. Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite. 2006;13:99–113.PubMedCrossRefGoogle Scholar
  5. 5.
    Mattiucci S et al. Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). J Parasitol. 1997;83:401–16.PubMedCrossRefGoogle Scholar
  6. 6.
    Paggi L, Mattiucci S, D’Amelio S. Allozyme and PCR-RFLP markers in anisakid nematodes, aethiological agents of human anisakidosis. Parassitologia. 2001;43 Suppl 1:21–7.PubMedGoogle Scholar
  7. 7.
    Jabbar A et al. Molecular characterization of anisakid nematode larvae from 13 species of fish from Western Australia. Int J Food Microbiol. 2013;161:247–53.PubMedCrossRefGoogle Scholar
  8. 8.
    Jabbar A et al. Molecular characterization of anisakid nematode larvae from 13 species of fish from Western Australia. Electrophoresis. 2012;33:499–505. Mutation scanning-based analysis of anisakid larvae from Sillago flindersi from Bass Strait, Australia.PubMedCrossRefGoogle Scholar
  9. 9.
    D’Amelio S et al. Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: ascaridoidea) defined by polymerase-chain-reaction-based restriction fragment length polymorphism. Int J Parasitol. 2000;30:223–6.PubMedCrossRefGoogle Scholar
  10. 10.
    Mattiucci S et al. Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae)s. Int J Parasitol. 2001;31:9–14.PubMedCrossRefGoogle Scholar
  11. 11.
    Paggi L, Nascetti G, Orecchia P, Mattiucci S, Bullini L. Biochemical taxonomy of ascaridoid nematodes. Parassitologia. 1985;27:105–12.PubMedGoogle Scholar
  12. 12.
    Gasser RB et al. Single-strand conformation polymorphism (SSCP) for the analysis of genetic variation. Nat Protoc. 2006;1:3121–8.PubMedCrossRefGoogle Scholar
  13. 13.
    Ishikura H et al. Anisakidae and anisakidosis. Prog Clin Parasitol. 1993;3:43–102.PubMedCrossRefGoogle Scholar
  14. 14.
    Audicana MT, Ansotegui IJ, de Corres LF, Kennedy MW. Anisakis simplex: dangerous—dead and alive? Trends Parasitol. 2002;18:20–5.PubMedCrossRefGoogle Scholar
  15. 15.
    Shamsi S et al. Occurrence and abundance of anisakid nematode larvae in five species of fish from southern Australian waters. Parasitol Res. 2011;108:927–34.PubMedCrossRefGoogle Scholar
  16. 16.
    Baird FJ, Gasser RB, Jabbar A, Lopata AL. Foodborne anisakiasis and allergy. Mol Cell Probes. 2014Google Scholar
  17. 17.
    Meeusen EN, Balic A. Do eosinophils have a role in the killing of helminth parasites? Parasitol Today. 2000;16:95–101.PubMedCrossRefGoogle Scholar
  18. 18.
    Galioto AM et al. Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval strongyloides stercoralis in mice. Infect Immun. 2006;74:5730–8.PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Gomez B et al. Eosinophilic gastroenteritis and Anisakis. Allergy. 1998;53:1148–54.PubMedCrossRefGoogle Scholar
  20. 20.••
    Nieuwenhuizen NE, Lopata AL. Anisakis—a food-borne parasite that triggers allergic host defences. Int J Parasitol. 2013;43:1047–57. A recent detailed review on the immunological reactions after exposure to Anisakis.PubMedCrossRefGoogle Scholar
  21. 21.
    Audicana MT et al. Recurrent anaphylaxis caused by Anisakis simplex parasitizing fish. J Allergy Clin Immunol. 1995;96:558–60.PubMedCrossRefGoogle Scholar
  22. 22.
    Del Pozo MD et al. Anisakis simplex, a relevant etiologic factor in acute urticaria. Allergy. 1997;52:576–9.PubMedCrossRefGoogle Scholar
  23. 23.
    Daschner A, Vega de la Osada F, Pascual CY. Allergy and parasites reevaluated: wide-scale induction of chronic urticaria by the ubiquitous fish-nematode Anisakis simplex in an endemic region. Allergol Immunopathol (Madr). 2005;33:31–7.CrossRefGoogle Scholar
  24. 24.
    Scala E et al. Occupational generalised urticaria and allergic airborne asthma due to Anisakis simplex. Eur J Dermatol. 2001;11:249–50.PubMedGoogle Scholar
  25. 25.
    Kirstein F et al. Anisakis pegreffii-induced airway hyperresponsiveness is mediated by gamma interferon in the absence of interleukin-4 receptor alpha responsiveness. Infect Immun. 2010;78:4077–86.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Nieuwenhuizen N, Herbert DR, Brombacher F, Lopata AL. Differential requirements for interleukin (IL)-4 and IL-13 in protein contact dermatitis induced by Anisakis. Allergy. 2009;64:1309–18.PubMedCrossRefGoogle Scholar
  27. 27.•
    Nieuwenhuizen N et al. Exposure to the fish parasite Anisakis causes allergic airway hyperreactivity and dermatitis. J Allergy Clin Immunol. 2006;117:1098–105. First detailed study to demonstrate sensitization to Anisakis among seafood processing workers and highlights possible sensitisation to Anisakis derived proteins in the absence of infection.PubMedCrossRefGoogle Scholar
  28. 28.
    Lopata AL, Jeebhay MF. Airborne seafood allergens as a cause of occupational allergy and asthma. Curr Allergy Asthm R. 2013;13:288–97.CrossRefGoogle Scholar
  29. 29.
    Caballero ML, Moneo I. Several allergens from Anisakis simplex are highly resistant to heat and pepsin treatments. Parasitol Res. 2004;93:248–51.PubMedCrossRefGoogle Scholar
  30. 30.
    Carballeda-Sangiao N et al. Identification of autoclave-resistant Anisakis simplex allergens. J Food Prot. 2014;77:605–9.PubMedCrossRefGoogle Scholar
  31. 31.
    Daschner A, Alonso-Gómez A, Cabanas R, Suarez-de-Parga JM, López-Serrano MC. Gastroallergic anisakiasis: borderline between food allergy and parasitic disease-clinical and allergologic evaluation of 20 patients with confirmed acute parasitism by Anisakis simplex. J Allergy Clin Immunol. 2000;105:176–81.PubMedCrossRefGoogle Scholar
  32. 32.
    Baeza ML, Zubeldia JM, Rubio M. Anisakis simplex allergy. ACI International. 2001;13:242–9.Google Scholar
  33. 33.
    Carretero Anibarro P et al. Protein contact dermatitis caused by Anisakis simplex. Contact Dermatitis. 1997;37:247.PubMedCrossRefGoogle Scholar
  34. 34.
    Montoro A, Perteguer MJ, Chivato T, Laguna R, Cuellar C. Recidivous acute urticaria caused by Anisakis simplex. Allergy. 1997;52:985–91.PubMedCrossRefGoogle Scholar
  35. 35.
    Pascual CY et al. Cross-reactivity between IgE-binding proteins from Anisakis, German cockroach, and chironomids. Allergy. 1997;52:514–20.PubMedCrossRefGoogle Scholar
  36. 36.
    Gamboa PM et al. Diagnostic utility of components in allergy to Anisakis simplex. J Investig Allergol Clin Immunol. 2012;22:13–9.PubMedGoogle Scholar
  37. 37.•
    Rodriguez-Perez R et al. Cross-reactivity between Anisakis spp. and wasp venom allergens. Int Arch Allergy Immunol. 2014;163:179–84. Provides data on the cross-sensitivity between the allergen Ani s 9 and wasp venom due to cross-reactive carbohydrates.PubMedCrossRefGoogle Scholar
  38. 38.
    Garcia F et al. Freezing protects against allergy to Anisakis simplex. J Investig Allergol Clin Immunol. 2001;11:49–52.PubMedGoogle Scholar
  39. 39.
    Baeza ML et al. Characterization of allergens secreted by Anisakis simplex parasite: clinical relevance in comparison with somatic allergens. Clin Exp Allergy. 2004;34:296–302.PubMedCrossRefGoogle Scholar
  40. 40.
    Moneo I et al. Isolation of a heat-resistant allergen from the fish parasite Anisakis simplex. Parasitol Res. 2005;96:285–9.PubMedCrossRefGoogle Scholar
  41. 41.
    Audicana MT, Kennedy MW. Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clin Microbiol Rev. 2008;21:360–79, table of contents.Google Scholar
  42. 42.••
    Fitzsimmons CM, Falcone FH, Dunne DW. Helminth allergens, parasite-specific IgE, and its protective role in human immunity. Front Immunol. 2014;5:61. This recent review compares dominant IgE-antigens in parasites with clinically important environmental allergens.PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Caballero ML et al. Isolation of Ani s 5, an excretory-secretory and highly heat-resistant allergen useful for the diagnosis of Anisakis larvae sensitization. Parasitol Res. 2008;103:1231–3.PubMedCrossRefGoogle Scholar
  44. 44.
    Chapman MD, Pomes A, Breiteneder H, Ferreira F. Nomenclature and structural biology of allergens. J Allergy Clin Immunol. 2007;119:414–20.PubMedCrossRefGoogle Scholar
  45. 45.
    Anadon AM et al. The Anisakis simplex Ani s 7 major allergen as an indicator of true Anisakis infections. Clin Exp Immunol. 2009;156:471–8.PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Moneo I, Caballero ML, Gomez F, Ortega E, Alonso MJ. Isolation and characterization of a major allergen from the fish parasite Anisakis simplex. J Allergy Clin Immunol. 2000;106:177–82.PubMedCrossRefGoogle Scholar
  47. 47.
    Shimakura K et al. Purification and molecular cloning of a major allergen from Anisakis simplex. Mol Biochem Parasitol. 2004;135:69–75.PubMedCrossRefGoogle Scholar
  48. 48.
    Rodriguez E et al. Novel sequences and epitopes of diagnostic value derived from the Anisakis simplex Ani s 7 major allergen. Allergy. 2008;63:219–25.PubMedCrossRefGoogle Scholar
  49. 49.
    Iglesias R, Leiro J, Santamarina MT, Sanmartin ML, Ubeira FM. Monoclonal antibodies against diagnostic Anisakis simplex antigens. Parasitol Res. 1997;83:755–61.PubMedCrossRefGoogle Scholar
  50. 50.
    Moneo I et al. Isolation of a heat-resistant allergen from the fish parasite Anisakis simplex. Parasitol Res. 2005;96:285–9.PubMedCrossRefGoogle Scholar
  51. 51.
    Rodriguez-Mahillo AI et al. Cloning and characterisation of the Anisakis simplex allergen Ani s 4 as a cysteine-protease inhibitor. Int J Parasitol. 2007;37:907–17.PubMedCrossRefGoogle Scholar
  52. 52.
    Rodriguez-Perez R, Moneo I, Rodriguez-Mahillo A, Caballero ML. Cloning and expression of Ani s 9, a new Anisakis simplex allergen. Mol Biochem Parasitol. 2008;159:92–7.PubMedCrossRefGoogle Scholar
  53. 53.
    Kobayashi Y, Shimakura K, Ishizaki S, Nagashima Y, Shiomi K. Purification and cDNA cloning of a new heat-stable allergen from Anisakis simplex. Mol Biochem Parasitol. 2007;155:138–45.PubMedCrossRefGoogle Scholar
  54. 54.
    Asturias JA, Eraso E, Moneo I, Martinez A. Is tropomyosin an allergen in Anisakis? Allergy. 2000;55:898–9.PubMedCrossRefGoogle Scholar
  55. 55.
    Guarneri F, Guarneri C, Benvenga S. Cross-reactivity of Anisakis simplex: possible role of Ani s 2 and Ani s 3. Int J Dermatol. 2007;46:146–50.PubMedGoogle Scholar
  56. 56.
    Lopata AL, Lehrer SB. New insights into seafood allergy. Curr Opin Allergy Clin Immunol. 2009;9:270–7.PubMedCrossRefGoogle Scholar
  57. 57.
    Kamath SD, et al. Molecular and immunological approaches in quantifying the air-borne food allergen tropomyosin in crab processing facilities. Int J Hyg Environ Health 2014.Google Scholar
  58. 58.
    Kamath SD et al. Effect of heat processing on antibody reactivity to allergen variants and fragments of black tiger prawn: a comprehensive allergenomic approach. Mol Nutr Food Res. 2014;58:1144–55.PubMedCrossRefGoogle Scholar
  59. 59.•
    Kamath SD, Abdel Rahman AM, Komoda T, Lopata AL. Impact of heat processing on the detection of the major shellfish allergen tropomyosin in crustaceans and molluscs using specific monoclonal antibodies. Food Chem. 2013;141:4031–9. Provides detailed data that heating has a profound effect on the detection of the major shellfish allergen tropomyosin, which could have considerable implications for the detection and quantification of other invertebrate tropomyosins in processed food.PubMedCrossRefGoogle Scholar
  60. 60.
    Abdel Rahman AM, Lopata AL, Randell EW, Helleur RJ. Absolute quantification method and validation of airborne snow crab allergen tropomyosin using tandem mass spectrometry. Anal Chim Acta. 2010;681:49–55.PubMedCrossRefGoogle Scholar
  61. 61.
    Moneo I, Caballero ML, Rodriguez-Perez R, Rodriguez-Mahillo AI, Gonzalez-Munoz M. Sensitization to the fish parasite Anisakis simplex: clinical and laboratory aspects. Parasitol Res. 2007;101:1051–5.PubMedCrossRefGoogle Scholar
  62. 62.
    Nieuwenhuizen NE et al. A cross-reactive monoclonal antibody to nematode haemoglobin enhances protective immune responses to Nippostrongylus brasiliensis. PLoS Negl Trop Dis. 2013;7:e2395.PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Feldmeier H, Poggensee G, Poggensee U. The epidemiology, natural history, and diagnosis of human anisakiasis. Eur Microbiol. 1993;2:30–6.Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.School of Pharmacy and Molecular Science, Centre for Biodiscovery and Molecular Development of TherapeuticsJames Cook UniversityTownsvilleAustralia
  2. 2.Department of ImmunologyMax Planck Institut fuer InfektionsbiologieBerlinGermany

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